Loss of functional diversity of ant assemblages in secondary tropical forests
Corresponding Editor: D. H. Feener, Jr.
Abstract
Secondary forests and plantations increasingly dominate the tropical wooded landscape in place of primary forests. The expected reduction of biodiversity and its impact on ecological functions provided by these secondary forests are of major concern to society and ecologists. The potential effect of biodiversity loss on ecosystem functioning depends largely on the associated loss in the functional diversity of animal and plant assemblages, i.e., the degree of functional redundancy among species. However, the relationship between species and functional diversity is still poorly documented for most ecosystems. Here, we analyze how changes in the species diversity of ground‐foraging ant assemblages translate into changes of functional diversity along a successional gradient of secondary forests in the Atlantic Forest of Brazil. Our analysis uses continuous measures of functional diversity and is based on four functional traits related to resource use of ants: body size, relative eye size, relative leg length, and trophic position. We find a strong relationship between species and functional diversity, independent of the functional traits used, with no evidence for saturation in this relationship. Recovery of species richness and diversity of ant assemblages in tropical secondary forests was accompanied by a proportional increase of functional richness and diversity of assemblages. Moreover, our results indicate that the increase in functional diversity along the successional gradient of secondary forests is primarily driven by rare species, which are functionally unique. The observed loss of both species and functional diversity in secondary forests offers no reason to believe that the ecological functions provided by secondary forests are buffered against species loss through functional redundancy.
Introduction
Current rates of extinction are estimated to be 100–1000 times greater than rates estimated for pre‐human periods (Lawton and May 1995, Pimm et al. 1995). In particular, tropical forests are likely to experience a large reduction in biodiversity should current trends in human activity continue. A major pressure on biodiversity is the destruction of primary tropical forests and their conversion into secondary habitats. The magnitude of loss in biodiversity depends on the ability of these secondary habitats to act as refuges for forest‐adapted species. The changes in species diversity due to destruction and conversion of tropical forest are relatively well documented, with most papers reporting a reduction in species diversity. Much less is known about the potential effects of species loss on ecosystem functions and services.
Experiments on relatively species‐poor assemblages indicate a positive relationship between species diversity and ecological functions (Naeem et al. 1995, McGrady‐Steed et al. 1997, Tilman et al. 1997). However, this link is neither strong nor universal (Díaz and Cabido 2001, Hooper et al. 2005, Petchey and Gaston 2006). Functional diversity has been defined as “the value and range of those species and organismal traits that influence ecosystem functioning” (Tilman 2001:109). It is emerging as an important aspect of biodiversity as it determines the strength and shape of the relationship between species diversity and ecosystem functions (Díaz and Cabido 2001). The degree to which species perform similar ecological functions in communities and ecosystems, i.e., the level of functional redundancy, is especially important for this relationship (Walker 1992, Lawton and Brown 1993). For example, if all species have an equal and additive effect on function (i.e., functional redundancy is low), one might expect a linear relationship between species diversity and the rate of ecosystem processes. If, on the other hand, many species are functionally redundant, the relationship between species diversity and ecosystem processes should become curvilinear. However, the relationship between species diversity and functional diversity in species‐rich, natural assemblages is poorly understood (Naeem 2002). To achieve the long‐term goal of restoring and managing sustainable ecosystems it is important to understand the linkages and mechanisms between species diversity and ecosystem processes, rather than focusing on species diversity as such (Walker 1992). High functional redundancy of species assemblages might indicate that ecosystem functions are robust to changes in diversity. This has important implications for the conservation of biodiversity and ecosystem functions in (regenerating) tropical forests.
A number of methods have been proposed for measuring functional diversity and richness (Tilman 2001, Mason et al. 2005, Petchey and Gaston 2006, Walker et al. 2008). Most ecological research has relied on the number of functional or trophic groups as a measure of functional diversity, though such approaches have disadvantages (Petchey and Gaston 2006). One disadvantage is the disregard for functional differences within organisms of the same group. More recently, measures of functional diversity have been proposed based on the large functional differences that delineate functional groups, as well as the smaller functional differences within these groups (Petchey and Gaston 2006, Walker et al. 2008). Regardless of the method, all measures of functional diversity suffer limitations. For example, the number and type of functional traits together with their correlations might alter the level of functional redundancy that assemblages appear to exhibit (Fonseca and Ganade 2001, Petchey and Gaston 2002b). Thus, research on the relationship between functional and species diversity must also evaluate the sensitivity of results to the functional traits used.
Here we focus on the functional diversity of ant assemblages (Hymenoptera: Formicidae) along a gradient of secondary succession in the Atlantic Forest of Brazil. From a functional perspective, ants play important roles in terrestrial ecosystems. Firstly, ants are unique because of their ubiquity and abundance in terrestrial ecosystems (Fittkau and Klinge 1973, Hölldobler and Wilson 1990, Tobin 1994). Secondly, ants interact with their environment by performing a variety of ecological functions. These include their functions as seed dispersers (Beattie 1985, Levey and Byrne 1993), predators (Kaspari 1996a, Philpott and Armbrecht 2006), and ecosystem engineers (Lobry de Bruyn and Conacher 1990, Folgarait 1998). In a meta‐analysis on faunal recovery in tropical secondary forest, Dunn (2004) found a general increase in ant diversity along gradients of forest succession (but see also Belshaw and Bolton 1993). It may take, however, several decades for the total recovery of community structure. We have demonstrated a similar pattern for the recovery of ant diversity in our study region in the Atlantic Forest of Brazil (Bihn et al. 2008a). For the same study region, ant behavior at baits indicates an abrupt shift from a preference for protein‐based baits in early successional stages to a preference for carbohydrate‐based baits in late‐successional stages of secondary forests, which might affect the functional composition of ant assemblages (Bihn et al. 2008b). Here we examine the relationship of species diversity to functional diversity of ant assemblages along the same gradient. Specifically, we address the following questions: (1) What is the relationship between species diversity and functional diversity in ant assemblages of tropical forests? (2) How do changes in species diversity along a gradient of regenerating tropical forests affect the functional diversity of ant assemblages?
Methods
Sampling of ants
The study was carried out in the Rio Cachoeira Nature Reserve (25°18′51″ S, 48°41′45″ W) located near the city of Antonina, in the coastal region of the Brazilian state of Paraná. Dense, ombrophilous lowland and submontane forests originally covered the area, but these suffered intense exploitation and large parts of them had been converted to pastures. The resulting landscape mosaic consists of old‐growth forests and secondary forests in various stages of succession (Ferretti and Britez 2006). Between June and September 2003 we sampled leaf litter ants in 12 study sites scattered across the reserve. The sites comprised a chronosequence of four stages of secondary forest succession, with three site replicates for each successional stage: very young secondary forest (4–6 years), young secondary forest (10–15 years), old secondary forest (35–50 years), and old‐growth forests (>100 years). Sites of secondary forests had been used as pastures for buffalo ranching, and site age is given as years after abandonment of ranching. Land use history for study sites was established through interviews with residents and reserve staff corroborated by inspection in a geographic information system (GIS) environment of high‐resolution, geocoded orthophotos from the years 1952, 1980, and 2002. Replicated sites of a particular successional stage were separated by an average distance of 4 km (range = 1–6 km). Replicated sites of a given successional stage were never situated in one continuous patch of the same vegetation type, but separated by areas of different successional stages, pastures, etc. (see Bihn et al. [2008a] for a map of the reserve and the location of the study sites within it).
At each study site we established two 50‐m transects (parallel, separated by 20 m) and collected leaf litter samples (from 1‐m2 quadrats) at 5‐m intervals along these transects (10 sampling points for each transect). This resulted in 20 samples for each site. Transects were located at least 50 m from any trail, pasture, or any other habitat in order to minimize edge effects. Ants were extracted from leaf litter, dead wood, and debris collected from the quadrats by sieving through a 1‐cm mesh screen and subsequently keeping the sifted material in Winkler bags for three days (see Agosti et al. [2000] for a detailed description of the method). All ants were examined and identified by J. H. Bihn. Many ants had to be assigned to morphospecies because they were undescribed or current systematic knowledge is insufficient to assign valid names. For morphospecies mentioned here, the genus name is followed by an epithet in the form “JHB00.” Otherwise, nomenclature follows Bolton (Bolton 1994, 2003). Voucher specimens are deposited at the Museu de Zoologia da Universidade de São Paulo, Brazil (MZUSP), and the State Museum of Natural History Karlsruhe, Germany (SMNK).
Southwood (1996) noted that terrestrial insect assemblages are continually challenged by a flow of transient species (also termed tourist, vagrant, or occasional species). The proportion of transient species is thought to be high in moist tropical forests (Stevens 1989, Longino et al. 2002). For a meaningful analysis one needs to exclude transient species, because these are not biologically associated with the sampled habitat (Magurran and Henderson 2003). Low numbers of individuals and/or low biomass in samples might indicate that a species had not established colonies in the (micro)habitat sampled and probably point to it being transient. Therefore, we excluded from all further analysis species that met at least one of the following criteria: (1) the number of individuals in all combined samples from a site was less than three and (2) the biomass (estimated from the number of individuals and head length with the formula given in Kaspari and Weiser [1999]) of all worker ants from all 20 samples combined was below 0.5 mg (see Appendix A).
The latter criterion is based on the intuitive idea that resource use of a species is proportional to total biomass. Therefore, the exclusion of species with the lowest biomass leads to assemblages dominated by species with a strong impact on resource use and ecosystem functions. The exact limit of 0.5 mg was arbitrary and mainly motivated by the minimum mass needed for the stable isotope analyses. Additionally, we excluded all army ants (Ecitoninae) from our analysis because their occurrence cannot be estimated in a reliable way with the sampling methods employed. We also excluded all males and queens from our analysis because these might never establish colonies after dispersal. This filtering of the original species lists did not qualitatively change the pattern of species richness along the successional gradient (see Appendix B).
Functional traits
Our intention was to assess the functional diversity of ant assemblages with regard to resource use. Four traits were therefore selected that represent (1) the quantity of resources consumed; (2) the mode of resource acquisition; and (3) the type of resources consumed. The functional traits measured for each species were as follows.
Body size.—
We used head length as a measure of total body size because of the strong correlation between head length and body mass (Kaspari and Weiser 1999). Body size is generally considered to be one of the most important attributes of an organism because it correlates strongly with many physiological, ecological, and life‐history traits (Peters 1983). Specifically, the body size of an organism determines the quantity of resources consumed. Head length was measured as the maximum longitudinal length from the most anterior part of the clypeus to the occipital margin, in full face view.
Relative eye size.—
Larger eyes offer a larger visual field and larger visual overlap of the fields. Ant species with large eyes have excellent vision and are very good at detecting moving objects (Via 1977, Wehner et al. 1983), whereas in ants with reduced eyes, optical cues are of minor importance for orientation and foraging. Eye size is also likely to correlate with the main foraging period (diurnal vs. nocturnal). We measured relative eye size as the ratio of eye length to head length.
Relative leg length.—
Longer legs allow faster and more efficient locomotion and foraging (Feener et al. 1988, Franks et al. 1999), but also increase their cross‐sectional area, which could prevent them from utilizing some foraging niches and types of shelter (Kaspari and Weiser 1999). Thus, relative leg length might yield information about the mode of resource acquisition. Relative leg length was measured as the ratio of leg length (combined length of femur and tibia) to head length.
Trophic position.—
Most leaf litter ants in tropical forests are thought to be omnivorous and opportunistic feeders, which harvest plant exudates, scavenge, and capture live prey as these are encountered (Hölldobler and Wilson 1990). However, for the majority of ant species the relative contribution of different food types to their diet is unknown. The analysis of stable isotope composition of organisms provides an alternative approach to assess their trophic position in food webs (Blüthgen et al. 2003, Davidson et al. 2003). A general result obtained from isotope studies is that consumers have relatively higher 15N/14N ratios than their prey. We accordingly used stable isotope data (i.e., 15N/14N ratios) to quantify the trophic position of ants.
Species and functional richness and diversity
We calculated functional diversity indices for the ant assemblage in each study site using two widely used indices, following the methods of Petchey and Gaston (functional diversity [FD]; Petchey and Gaston 2002b, 2006) and Walker et al. (functional attribute diversity [FAD]; Walker et al. 1999). Previous studies on the functional composition of ant communities have used the classification of ants into functional groups (e.g., Andersen 1995, 1997). We decided to use continuous measures of functional diversity for two reasons: first, these measures do not require an arbitrary assignment of species into categories (Simberloff and Dayan 1991); second, continuous measures of functional diversity include the functional differences between species within functional groups as well as the differences among functional groups (Petchey and Gaston 2002b).
For the computation of FD, the species by trait matrix was converted into a distance matrix, and this was clustered to produce a dendrogram. We used z‐standardized values to assign all functional traits equal importance in our analysis. The FD of an assemblage is defined as the combined length of all branches in this dendrogram. The choice of distance and clustering method for the calculation of FD may greatly affect the FD values. Thus, we tested several distance and clustering methods (including consensus trees), then selected the most reliable tree for the calculation of FD based on the cophenetic correlation between pairwise distances in trait space and pairwise distances across the dendrogram (see Mouchet et al. [2008] for the distance and clustering algorithms used and details of the method). The combination of Euclidean distances and the unweighted pair group centroid method (UPGMA) yielded the strongest cophenetic correlation (0.85) and were used throughout our analysis. The FAD of an assemblage is the total of all pairwise distances between species in functional trait space. Again, we used Euclidean distances as a measure of dissimilarity.
In their original form, both indices of functional diversity weight every species in a given assemblage equally, i.e., they do not take into account the relative abundance of species. These unweighted indices are therefore measures of functional richness. For exploration of the relationship between functional richness and species richness we used the (unweighted) FD index and the observed species richness per site. For the calculation of functional and species diversity we applied a rarefaction technique to the FD index and species richness. This resulted in indices that account for evenness in species assemblages. The contribution of each species of an assemblage is weighted by its relative number of occurrences per site, i.e., the number of samples (n = 20) per site in which it was recorded.
We plotted values of functional richness and diversity against species richness and diversity and tested for saturation using multiple regression with species richness and quadratic species richness as predictor variables. The analysis was repeated for the relationship between species and functional richness using different combinations of only three of the four functional traits to evaluate whether our results were robust with respect to the number and combination of functional traits considered.
Functional diversity during forest succession
For the comparison of functional diversity indices among ant assemblages we followed the functional rarefaction method as proposed by Walker et al. (2008). As an improvement of Sanders' (1968) rarefaction method, Hurlbert (1971) introduced the idea of using the expected number of species in a sample of n individuals drawn at random from the pool of N individuals as a measure of species diversity. Since each n defines a separate diversity measure, a family of diversity measures can be obtained with the rarefaction technique. For a sample size of n = 2 this measure is equivalent to the Simpson diversity index (Smith and Grassle 1977). Simpson's index is relatively unaffected by rare species. As the rarefied sample size n increases from 2, diversity indices are obtained that are progressively more sensitive to rare species. This property of the indices can be used to understand the contribution of rare and common species to diversity. Walker et al. (2008) generalize the rarefaction technique from species diversity studies and apply it to the functional diversity indices FD and FAD. The effect of rarefied sample size on the sensitivity to rare species is preserved in this generalization of the rarefaction technique. Functional rarefaction transforms the unweighted indices FD and FAD into a family of weighted indices and corrects for sample‐size‐induced bias.
For each ant assemblage we calculated the expected species diversity 〈Sn〉, the rarefied functional attribute diversity index 〈FADn〉, and the rarefied functional diversity index 〈FDn〉 for n = 2 and n = 59 occurrences. The number of species occurrences varied from site to site and 59 occurrences was the ant assemblage with the smallest sample size (range = 59–282). Given that 〈FD2〉 = 2〈FAD2〉 (Walker et al. 2008), we did not calculate 〈FD2〉. Note that we used formulas and algorithms for abundance‐based rarefaction (sensu Walker et al. 2008), which means that we treated each species occurrence as an individual in these calculations.
We made use of the following three properties of the calculated rarefied indices for the interpretation of the results (Walker et al. 2008). First, the functional diversity indices 〈FAD2〉, 〈FAD59〉, and 〈FD59〉 are sensitive to the differences in the functional traits of species whereas the indices of expected species diversity 〈S2〉 and 〈S59〉 are not. Second, the rarefaction to different numbers of occurrences gives way to the evaluation of the sensitivity to rare species: 〈S59〉, 〈FAD59〉, and 〈FD59〉 are more sensitive to rare species than 〈S2〉 and 〈FAD2〉. Third, Petchey and Gaston (2006) emphasize that FD is insensitive to functionally redundant species whereas 〈FAD2〉, 〈FAD59〉, 〈S2〉, and 〈S59〉 are sensitive to these.
Results
Our analysis was based on 2212 occurrences of 99 species (30 genera) in 12 sites. Ant species covered a wide range of values for the functional traits measured. For example, the mean head length of the smallest ant (0.34 mm; Brachymyrmex JHB02) was almost eight times smaller than that of the largest ant (2.67 mm; Odontomachus haematodus). Mean δ15 N values ranged from 1.94 (Acropyga fuhrmanni) to 10.8 (Amblyopone armigera). Studies on insects generally report a δ15 N enrichment of 2–3‰ per trophic level (McCutchan et al. 2003). Thus, ant species in our study covered about three trophic levels. The functional dendrogram describes the functional relationships among ant species (Fig. 1). This plot highlights that a number of sets of species are functionally very similar, so that if they are present in the same local assemblage they will be redundant with respect to one another. Other species had a very uncommon combination of functional traits, e.g., Pheidole lucretii or Amblyopone armigera. These species always increased the functional diversity of assemblages irrespective of which other species were present.
